Nitrogen Cycling in Flooded Taro Agriculture

Soil and Crop Management
December 2013
SCM-31

Nitrogen Cycling in Flooded Taro Agriculture

Jonathan L. Deenik1, C. Ryan Penton2, and Greg Bruland3
1Department of Tropical Plant and Soil Sciences, University of Hawai‘i-Mänoa

2Center for Microbial Ecology, Michigan State University
3Department of Biology and Natural Resources, Principia College

Nitrogen (N) is an essential element in plant nutrition Figure 1. Lo‘i kalo production in the fertile soils of Hanalei
that is often a limiting factor in taro production Valley on the Island of Kaua‘i.
systems. Efficient management of N is critical to ensure
growers achieve target yields while simultaneously and volatilization). The transformations depend on a
protecting valuable water resources. Insufficient N number of environmental factors including oxygen
limits taro yields, whereas excess fertilizer N impairs status, pH, temperature, amount of organic matter, and
water quality, with adverse effects on fragile fresh and microbial population.
marine water ecosystems. Nitrogen cycling in flooded
agroecosystems is complex and difficult to predict. The Nitrogen Forms and the N Cycle
purpose of this publication is to present an overview Nitrogen in a taro system exists as inorganic dissolved
of the N cycle in a flooded environment, with a focus ions (ammonium, or NH4+, and nitrate, or NO-3), more
on the fate of plant-available N. This publication uses complex organic molecules associated with soil organic
data gathered from field measurements and laboratory matter, and gaseous N. Taro roots take up dissolved
experiments conducted in Hawai‘i to illustrate specific
pathways within the N cycle in flooded taro. With a
better understanding of this complex system, farmers
and agricultural professionals will be better placed to
improve N fertilizer use.

The Flooded Taro Environment
The flooded taro environment consists of four distinct
but interconnected zones: (1) the air above the ponded
water, (2) the overlying surface water, (3) the thin
aerobic surface soil layer, and (4) the anaerobic subsoil
layer (Fig. 2). The diagram shows that N is subject to a
number of different transformations depending on its
form and location within the different zones. Some of
the transformations represent potential gains in plant-
available N (mineralization and biological nitrogen
fixation, or BNF), while others are losses (denitrification

Published by the College of Tropical Agriculture and Human Resources (CTAHR) and issued in furtherance of Cooperative Extension work, Acts of May 8 and June 30, 1914, in co-
operation with the U.S. Department of Agriculture, under the Director/Dean, Cooperative Extension Service/CTAHR, University of Hawai‘i at Mānoa, Honolulu, Hawai‘i 96822.
Copyright 2011, University of Hawai‘i. For reproduction and use permission, contact the CTAHR Office of Communication Services, [email protected], 808-956-7036. The university is
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UH–CTAHR Nitrogen Cycling in Flooded Taro Agriculture SCM-31 — Dec. 2013

inorganic N primarily as NexHte4+,ntwNhOic3-h. is the dominant collectively represent the N cycle (Fig. 2). Primary N
ionic form, and to a lesser The largest pool inputs (gains) into the taro system include the following:
1) organic and conventional fertilizers; 2) incorporation
of N in the soil occurs as organic N in the form of amino of crop residues, green manure residues, and organic
matter; 3) BNF; and 4) N in irrigation water. Potential
acids, amines, proteins, and larger humic compounds. In N losses from the system include the following: 1)
N removed by the crop via root uptake; 2) N losses
large part, these compounds are not directly available for through water outflow from the field or leaching into the
groundwater; and 3) losses through various chemical and
uptake by taro roots and must be converted into inorganic biochemical transformations, including denitrification
and volatilization.
forms before they can be used by plants. Nitrogen can

also exist in gaseous forms as a component of ammonia

(NH3), di-nitrogen (N2), and nitrous oxide (N2O).
The form of N at any given time depends on a

number of soil chemical and biochemical processes that

Figure 2. Processes controlling the transformations of N in the surface water and aerobic and anaerobic
soil layers in a flooded taro system. Red text represents losses of plant-available N, and green text repre-
sents additions of plant-available N (drawing adapted from Mitsch and Gosslink (2007) and Reddy (1982)
(taro art by Solomon Enos).
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UH–CTAHR Nitrogen Cycling in Flooded Taro Agriculture SCM-31 — Dec. 2013

Role of Oxygen matter tends to reduce dissolved O2 concentrations
The oxygen (O2) status of the water and sediment because the high organic matter stimulates microbial
layers plays a key role in determining potential activity and O2 consumption.

N-transformation pathways. In the presence of O2
(aerobic conditions), oxidizing reactions pNreOd3-3o. mI ninat htee, Nitrogen Transformations in Soils
resulting in the conversion of NH4+ to N-mineralization: Nitrogen in soil exists primarily

absence opfroOm2 (oatninagerothbeicgcaosnedoiutisonlos)s,sreodfuNcin(gi.ec.o,nNdiOti3-ontos ramesaicodrrioglyoarncgiocannvNiesrmitnesdtahisenttsohoeiilnyoobrrggreaaannkiiccdNmowa(tNnteHro.4+rOgaanrngdaicNniOmc 3-3aN)ttbeiysr
prevail,

N2O). Typically, the overlying water is aerobic because
it is in equilibrium with atmospheric O2. In situ O2 to get energy. The conversion process, termed N

measurements performed at four different taro farms mineralization, represents an important source of plant-

on Kaua‘i, O‘ahu, and Hawai‘i Islands showed that O2 available N. Nitrogen mineralization occurs under both
concentration in the overlying water ranged from 1.99
aerobic and anaerobic conditions, although it proceeds

to 8.57 mg L-1 with a mean value of 5.74 mg L-1. Aquatic more rapidly in the presence of Oo2n.lyInptrhoedaubcseesncNeHo4+f,
O2, the minera lization process
life becomes stressed when dissolved O2 concentrations
drop below 5 mg L-1. The soil layer consists of two zones: which is available for plant use. The capacity of a soil to

an aerobic layer at the soil–water interface where O2 is mineralize N is called N-mineralization potential. The
replenished from the overlying water column, producing
amount of organic matter in the soil and how the soil

oxidizing conditions, and an underlying anaerobic zone is managed are two critical factors determining a soil’s

characterized by reducing conditions. The aerobic layer N-mineralization potential. Taro soils under organic

is generally thin (<1 cm), but its relative thickness can management tend to have higher concentrations of total N

show considerable variability across sites. Figure 3 and exhibit higher N-mineralization potentials compared

shows an example of how the O2 status in taro fields to soils under conventional management. The graph in
can vary. In the first example (Lo‘i 1), O2 penetrates into
the surface soil layer, maintaining aerobic conditions Figure 4 depicts the N-mineralization potential of a taro

soil under conventional fertilizer management (red) and

to a depth of 3 mm. On the other hand, Lo‘i 2 shows another under organic management (green). The soil that

a situation where anaerobic conditions begin within a had received organic fertilizers for more than 10 years

millimeter above the soil surface and persist throughout shows a much higher potential to mineralize N than the

the soil layer. The presence of high levels of organic conventionally managed soil. These data highlight the

Figure 3. Range of measured dissolved O2 in the flood- Figure 4. Nitrogen-mineralization potentials of two Hanalei
waters and sediment of cultivated lo‘i. series lo‘i soils as affected by type of soil management.

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UH–CTAHR Nitrogen Cycling in Flooded Taro Agriculture SCM-31 — Dec. 2013

important role organic inputs play in maintaining a soil’s
ability to supply NH4+4. Enhancing soil organic matter
increases N-mineralization potential and can reduce N
inputs from fertilizer.

Nitrification: Nitrification is tthheenbioNcOh3e-mmiecdailactoendvbeyrsitohne
of NH4+ to produce NO2 and
soil bacteria Nitrosomonas and Nitrobacter. The reaction

can only occur in the presence of O2 and proceeds in two
steps, as follows:

NH4+  +  1½O!   !"#$%&%'%()& NO2-­‐  +  2H+  +  H2O  +  275kJ   EQN 1

NO2-­‐  +  ½O!   !"#$%&'(#)$ NO3-­‐  +  76kJ   EQN 2

Ammonium in the aerobic tsouNrfOac-3ethwroautegrh and surface Figure 5. The stem of an aquatic plant showing presence
sediment is readily converted nitrification. of hollow arenchyma that act as conuits of atmospheric
O2 into the rhizosphere.
Nitrification can also occur in the oxidized rhizosphere
it is rapidly denitrified. Recent sampling across a range of
of taro grown in flooded soils (Figure 2). Similar to other taro fields in Hanalei and Waiähole found that nitrifying
and denitrifying bacteria are present in large numbers
wetland plants, taro transports atmospheric O2 through and active. Comparisons between conventionally and
its stem down into the subsoil, where the O2 diffuses out organically managed taro fields indicate that taro fields
of the roots into the sIonil,aecrroeabtiicngenavitrhoinnmaeernotsbitchreegNioOn3- receiving conventional fertilizers show a much higher
adjacent to the root. denitrification potential than taro fields under organic
management.
can accumulate and serve as a pool of plant-available
Rhizosphere nitrification and denitrification: As
N. However, at aerobic and anaerobic interfaces such as discussed earlier, taro sediments are mostly anaerobic,
except for a thin aerobic surface layer and aerobic soil
tthhoesNeOc-o3 hmams oantleyndfoeunncyd in a flooded taro environment, regions adjacent to taro roots. Taro stems, like the
to diffuse into anaerobic layers stems of other wetland plants, contain hollow channels
(arenchyma) that act as conduits transporting air from
where it is rapidly lost through denitrification. the atmosphere down to the root-zone (Fig. 5). Oxygen
transported through the plant ends up in the root tissue,
Denitrification: Denitrification is a stepwise series of where some of it diffuses out into the adjacent sediment,
producing a thin zone of aerobic soil, surrounded by
reduction reactions tchaartriceodnovuetrtbsyplaandti-vaevrasielagbrloeuNp Oof3- the anaerobic bulk soil. Using an O2 microelectrode, we
anaerobic bacteria have demonstrated that the aerobic zone can extend as
much as 2 mm from the taro root. In a whole-core taro
into gaseous N (N2O or N2) that eventually escapes experiment, we measured significant losses of plant-
from the soil and enters the atmosphere. Nitrous oxide available NH4+ through the coupling of nitrification and
denitrification in the rhizosphere of taro plants (Penton
is an important greenhouse gas with 300 times the et al. 2013) (Fig. 6). In the aerobic rhizosphere, nitrifying

dheenati-ttrriafypipnigngbaccatpearciaityreoadf iClyOu2.seInNtOh3-e absence of O2,
as the terminal

electron acceptor as they obtain energy from organic

matter. The reaction is as follows:

2NO-3­‐   !! O  NO-2­‐     !! O 2NO↑   ! O  N  2O↑ ! O   N! ↑ EQN 3

TanhaeerdobenicitinritfeircfaactieownhreereacNtOio3-nproocdcuucresd at the aerobic–
from nitrification

in aerobic soil regions (surface sediments and the

rhizosphere) diffuses into adjacent anaerobic zones where

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UH–CTAHR Nitrogen Cycling in Flooded Taro Agriculture SCM-31 — Dec. 2013

bacteria readily convert NH4+ to NO3-, which is either taken photosynthesis rates increase, reducing dissolved CO2
up by taro roots or adnifafeursoebsicinztoonteh,eNadOj3a- ciesnrtaapnidaleyrolboisct concentrations and thus causing a steady rise in water pH.
zone. Once in the Sampling several taro fields in Hanalei Valley confirmed
a rise in water pH between morning and afternoon.
through denitrification. Through careful experiments we Samples collected between 8 and 10 AM showed a mean
have found that as much as 35% of NH4+ in the subsoil pH of 6.2, while samples collected at the same locations
can be lost through the coupling of nitrification and between 1 and 3 PM showed a distinct rise to 8.0, with
maximum pH values measured at 9.1 (Fig. 7). Overall, the
denitrification in the rhizosphere. Other experiments have data indicate that afternoon increases in the floodwater
pH in young taro fields produce conditions that are more
shown that nitrification/denitrification reactions in the favorable for the loss of plant-available NH4+ through
volatilization. On the other hand, in mature taro fields,
rhizosphere of flooded rice plants are also a significant where the leaf canopy shades the water throughout the
pathway for the loss of plant-available NH4+. day, water pH remains below 7 consistently.

Ammonia volatilization: Ammonium dissolved in the Anammox: Anaerobic ammonium oxidation (anammox)
involves the anaerobic oxidation of NH4+ coupled with
water can be converted into NH3 gas through a process NO2 reduction to create N2 gas. The reaction is mediated
called ammonia volatilization, representing a loss of obsexydicaimsguerronfutaplcaeyoeflaraysu.etrTo, htcreoouppphrleiecsdebnwacciettheorNfiaONt3-H3hra4+etadinundchtaNiobOnit3-3taoinnNotxOhiec2
in adjacent anoxic layers, is a prerequisite condition
plant-available N. The conversion process is controlled that provides a consistent supply of NO2 for anammox
bacteria. Anammox was first documented in wastewater
by the pH of the overlying water. At pH 7.0 or less, for treatment facilities in the Netherlands in the early
example, NH4+ 1990s, and it has since been found in a broad range
volatilization. is stable in water, and it is not subject to of environments, including river sediments, wetlands,
As pH rises, however, NH4+ converts to and paddy rice fields in Asia. A survey of flooded taro

NH3 and is lost to the atmosphere. The volatilization
reaction increases sharply when pH rises above 8.5, with

as much as 35% loss at pH 9. The pH of the overlying

water column in flooded taro fields can vary widely

from acidic (<6) to alkaline (>9) conditions between the

morning and afternoon. This large daily fluctuation of pH

is due primarily to algal growth and consumption of CO2
during photosynthesis. During the morning hours when

photosynthesis is low due to lack of sunlight, dissolved

CO2 keeps the water acidic. As the day progresses, algal

N2O,
 N2
 
 
denitrification

 
 
 

 

 
-­‐

   
 

NO3-­‐ diffusion 3

  +
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 NO

 
 
 
 
 
 
 
NH4+
diffusion NH
 
  aznoanereobic
4

 
aznoanereobic zaoernoebic
 
 

 
 

 


 
 
 
 root

 
  zaoernoebic

Figure 6. The presence of an aerobic zone surrounding Figure 7. Time of day effects on water pH in taro fields
taro roots allows for the coupling of nitrification and de- of Hanalei Valley.
nitrification in the subsoil of flooded taro fields.

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UH–CTAHR Nitrogen Cycling in Flooded Taro Agriculture SCM-31 — Dec. 2013

sediments from O‘ahu (Waiähole and Hale‘iwa) and N more gradually over time. Organic materials tend to
Kaua‘i (Hanalei) confirmed the presence of anammox release N into NH4+ form at a slower rate than soluble
bacteria, but incubation experiments using the isotope- synthetic fertilizers, thus reducing potential for losses.
pairing technique revealed that the anammox reaction In addition, organic materials are much more than just
was not contributing significantly to NH4+ loss. Similarly, suppliers of N. They are typically good sources of P, Ca,
anammox activity in paddy rice fields in Japan and S, and the micronutrients, and they provide added benefits
China showed the presence of anammox bacteria, to the physical, chemical, and biological properties of soil.
but isotope-pairing experiments showed negligible
contributions to N loss. These results suggest that Timing and Placement: Currently, most commercial
anammox is not a contributor to N loss in managed
flooded agroecosystems. taro farms apply a small portion of N as a pre-plant

application prior to flooding, with the remaining N

broadcast as urea or ammonium sulfate granules into

Nitrogen Management the flooded taro fields at monthly intervals through the
Nitrogen inputs play an important role in the production
of wetland taro. Efficient management of N fertilizers first six months of production. The fertilizer pellets sink
must consider the source of N, its application rate, the
timing of application, and its placement in the field. and come to rest in the aerobic zone on the sediment
surface where they dissolve rapidly, releasing NH4+which
is then subject to a number of potential loss pathways
(Fig. 8). If the floodwater pH is high (>8), NH44+is readily
Nitrogen Source: Taro plants preferentially use the NH4+ pvorelasteinliczeedoftoON2,HN3 Hga4+sisanrdapliodsltytocothnevaetrmteodspinhteoreN. OIn3-tbhye
form of N, and therefore ffeerrttiilliizzeerrsmcaotemripaolssethdatorfelNeaOs3-e. dssoueibnlsibtoraiiclf.ticeTarhitaiior(dnnliytar,sidfitichsasetoiNolvnOe)d3-anNddiHfsf4+uuabsnseedsqNiunOetno3-3tltiyhneltohsaetntashuerrroofuabgcihec
NH4+ are preferred over sediment readily diffuse into the floodwaters and can

There are many types of N fertilizers available to taro

growers, including soluble synthetic products and many

organic amendments. Synthetic products such as urea

(46-0-0) and blended fertilizers (16-16-16, 10-10-10, etc.) exit the taro field and pose a downstream contamination

are commonly used in conventional taro fields because threat. For all of these reasons, it is recommended that
they contain soluble urea that readily hydrolyzes to NH4+
when added to the flooded soil. Ammonium sulfate (21- N fertilizers be applied to the subsoil of flooded taro

fields. Placing the fertilizer in the subsoil is preferable

0-0) is another synthetic fertilizer commonly used in for the following reasons: 1) N is conserved in the
NthHe 4+4pofoternmti;al2)fonritdreifniictaritfiiocnatiiosnm; 3in)
taro production. Urea-based fertilizers and ammonium imized, reducing
sulfate provide a rapidly available source of NH4+ that is subsoil pH tends
easily used by taro roots. Nitrate-containing fertilizers
to be below 7, preventing N loss through ammonia

such as CaNO3 (15.5-0-0, 19% Ca) and KNO3 (13-0-46), volatilization; and 4) reactive forms of N, primarily
NH4+, is kept separate from overlying waters, reducing
winhfilloeowdeedll-ssouiiltsedbefcoarusderytlhaendNOcr3-ofposr,maroef not effective potential for downstream contamination. Controlled-
N is quickly

denitrified to N2 gas when it moves into the anaerobic release conventional fertilizers or organic amendments
release NH4+ more slowly than urea, and thus can be
NseOdi3-m-beansetsd common in flooded taro fields. Applying added as a one time amendment to the subsoil prior to
fertilizers is not recommended for wetland

taro production. Organic fertilizers such as feather planting and supply adequate N to taro during the first

meal, blood meal, fish meal, and chicken manure are six months of the crop. In addition to the environmental
sources of NH4+.
good waste materials Organic forms of N in animal- benefits, a one-time pre-plant fertilizer application
based are readily mineralized into NH4+
offers an opportunity to reduce labor costs associated

under both flooded and dryland conditions. Nitrogen- with monthly urea applications.

rich materials (feather meal, blood meal, fish meal) are
relatively rapid sources of NH4+, whereas steer manure,
green waste, and low-N compost materials supply less

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UH–CTAHR Nitrogen Cycling in Flooded Taro Agriculture SCM-31 — Dec. 2013

Summary forms, in the subsoil conserves N in the preferred NH4+
Nitrogen is subject to a number of transformation pathways form, reducing losses to volatilization and denitrification

in flooded soils, some of which increase its availability and minimizing N contamination of downstream

for plant use (i.e., mineralization and nitrification) while environments. Controlled-release forms of synthetic

others decrease availability (ammonia volatilization fertilizers and organic amendments applied to the subsoil
upsreimNaHry4+
and denitrification). Taro plants preferentially one time prior to planting provide the following potential
in flooded soils, but NH4+ is subject to three opfrNotHec4+ttioonthoefsNoilininthsyenNchHr4+ofnoyrmwiitnh
loss pathways – ammonia volatilization, coupling of benefits: slow release
taro N requirements;

nitrification and denitrification, and loss in outflow the subsoil, reducing potential losses; and a reduction in

water. Placing fertilizers, both conventional and organic labor time associated with monthly applications of urea.

Figure 8. Nitrogen fertilizers (red dots), synthetic or organic, placed in aerobic zones (surface water and
aerobic soil surface layers) are subject to reactions (nitrification + denitrification and volatilization) that
increase likelihood of loss. Fertilizers placed in the anaerobic subsoil (green dots) are exposed to fewer
potential loss pathways.

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UH–CTAHR Nitrogen Cycling in Flooded Taro Agriculture SCM-31 — Dec. 2013

References Acknowledgements
Mitsch, W.J., and J.G. Gosselink. 2000. Wetlands. 3rd We thank Roy Yamakawa (Kaua‘i County Cooperative
Extension Service) for his assistance in the field and
ed. New York: John Wiley and Sons. strong connections with the taro-farming community
Reddy, K.R. 1982. Nitrogen cycling in a flooded-soil of Kaua‘i County. A special thanks to the cooperating
taro farmers from Waiähole Valley and Hale‘iwa on
ecosystem plamnted to rice (Oryza sativa L.). Plant O‘ahu and Hanalei Valley on Kaua‘i. We are grateful to
and Soil 67:209–220. Jackie Mueller and Gavin Brown for their assistance in
Penton, C.R., J.L. Deenik, B.N. Popp, G.L. Bruland, P. the laboratory and field. This research was supported in
Engstrom, D. St Louis, G.A. Brown, and J. Tiedje. part by a grant from the United States Department of
2013. Importance of sub-surface rhizosphere- Agriculture National Institute of Food and Agriculture
mediated coupled nitrification-denitrification in a (award 2008-35107-04526) and HATCH funds (18-827).
flooded agroecosystem in Hawaii. Soil Biology and
Biochemistry 57: 362–373.

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